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Serological Survey of Hantavirus In Rodents From Prairie Dog Ecosystems In
Chihuahua, Mexico
Author(s): Karla Moreno-Torres, Fernando Gual-Sill, Ricardo Morales-Jiménez, André V. Rubio,
Gerardo Ceballos, and Gerardo Suzán
Source: The Southwestern Naturalist, 59(4):590-594.
Published By: Southwestern Association of Naturalists
DOI: http://dx.doi.org/10.1894/SGM-37.1
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THE SOUTHWESTERN NATURALIST 59(4): 590–594
DECEMBER 2014
NOTE
SEROLOGICAL SURVEY OF HANTAVIRUS IN RODENTS FROM
PRAIRIE DOG ECOSYSTEMS IN CHIHUAHUA, MEXICO
KARLA MORENO-TORRES,* FERNANDO GUAL-SILL, RICARDO MORALES-JIMÉNEZ, ANDRÉ V. RUBIO, GERARDO CEBALLOS,
AND GERARDO SUZÁN
Departamento de Etologı́a, Fauna Silvestre y Animales de Laboratorio, Facultad de Medicina Veterinaria y Zootecnia,
Universidad Nacional Autónoma de México, Ciudad Universitaria, C.P. 04510 Distrito Federal, México (KMT, AVR, GS)
Departamento de Enfermedades Emergentes, Instituto de Diagnóstico y Referencia Epidemiológicos, Secretarı́a de Salud,
Prol. de Carpio No. 470, Distrito Federal, C.P. 11340, México (RMJ)
Departamento de Producción Agrı́cola y Animal, Universidad Autónoma Metropolitana, Calzada del Hueso 1100,
Distrito Federal, C.P. 04960, México (FGS)
Instituto de Ecologı́a, Universidad Nacional Autónoma de México, Ciudad Universitaria, Distrito Federal, C.P. 04510, México (GC)
Present address of KMT: Department of Veterinary Preventive Medicine, The Ohio State University, 1920 Coffey Road,
Columbus, OH 43210
*Correspondent: irazema.moreno@gmail.com
ABSTRACT—In northwestern Mexico, studies on hantavirus in rodent hosts are scarce. Our objective was to
conduct serological tests to detect antibodies against hantavirus in rodents from the Janos–Nuevo Casas
Grandes prairie dog complex (JCGC) in northwestern Mexico. In December 2007 and April 2008, we captured
149 rodents and tested for immunoglobulin G antibodies to New World hantaviruses. Three Peromyscus
maniculatus from grassland habitats without prairie dog colonies were antibody positive. This is the first record
of hantavirus prevalence in wild rodents from JCGC and from the state of Chihuahua. Further molecular
analysis is needed to describe which hantavirus is circulating in this area.
RESUMEN—En el noroeste de México los estudios sobre hantavirus en roedores hospederos son escasos.
Nuestro objetivo fue realizar un estudio serológico con el fin de detectar anticuerpos contra hantavirus en
roedores del complejo de perros llaneros Janos–Nuevo Casas Grandes (CJCG), ubicado en el noroeste de
México. En diciembre de 2007 y abril de 2008, capturamos 149 roedores y los analizamos para la presencia de
anticuerpos IgG a hantavirus del Nuevo Mundo. Tres Peromyscus maniculatus de los pastizales sin colonias de
perros llaneros fueron positivos a hantavirus. Este es el primer registro de la prevalencia de hantavirus en
roedores silvestres en el CJCG y en el estado de Chihuahua. Estudios adicionales con análisis moleculares se
deben realizar para conocer qué hantavirus se encuentra circulando en esta área.
Hantaviruses (family Bunyaviridae, genus Hantavirus)
have emerged as an important rodent-borne zoonosis that
is distributed globally (Jonsson et al., 2010). These viruses
are the etiological agents of hemorrhagic fever with renal
syndrome in Eurasia (Old Word hantaviruses) and
hantavirus pulmonary syndrome (HPS) in the Americas
(New World hantaviruses; Jonsson et al., 2010). The first
human cases in the Americas were recognized in 1993 in
the southwestern United States (Childs et al., 1994). Since
then, cases of HPS have been reported in Central and
South America (e.g., Hjelle et al., 1996; Fulhorst et al.,
1997; Toro et al., 1998; Vincent et al., 2000). Currently,
more than 40 genotypes of hantaviruses have been
reported in the Americas; 20 of these are associated with
diseases in humans (Hjelle and Torres-Pérez, 2010).
Commonly, each unique virus type is maintained in
nature by a single rodent host species in which it causes a
chronic infection that may be largely asymptomatic
(Jonsson et al., 2010). The transmission of hantavirus
within host populations is believed to occur mainly
through aggressive encounters between rodents (Mills et
al., 1997; Klein et al., 2004).
Although there have been no human cases of HPS to
date in Mexico (Vázquez-Pérez et al., 2012), four
hantaviruses have been documented in rodents that
occur in Mexico: El Moro Canyon virus, Playa de Oro
virus, Limestone Canyon virus, and Sin Nombre virus
(Hjelle et al., 1995; Chu et al., 2008; Milazzo et al., 2012),
December 2014
Note
with antibody prevalences ranging between 4% and 9% of
samples tested. Additionally, three possible new hantaviruses were described recently: Carrizal virus, Huitzilac
virus, and Montano virus (Kariwa et al., 2012). However,
these strains may be members of Limestone Canyon virus
(Montano virus) and El Moro Canyon virus or Rio
Segundo virus (Carrizal virus and Huitzilac virus; Milazzo
et al., 2012). Of these viruses, only Sin Nombre virus is
known to cause HPS. Serological surveys of hantaviruses
have been conducted in several areas of Mexico (e.g.,
Mantooth et al., 2001; Suzán et al., 2001; Castro-Arellano
et al., 2009), though little is known about hantavirus
prevalence in rodents from the northwestern portion of
Mexico. Northwestern Mexico has environmental conditions similar to areas of the United States where HPS cases
have occurred (Yates et al., 2002) and where rodents show
molecular and serological evidence of hantavirus (e.g.
Childs et al., 1994; Mills et al., 1998, 1999). The purpose
of this study was to perform a serological survey on the
Janos–Casas Grandes prairie dog complex (JCGC; Ceballos et al., 1993) in the previously unexamined state of
Chihuahua, Mexico. We wanted to investigate hantavirus
prevalence in wild rodents that inhabit this protected area
that is part of one of the largest continuous black-tailed
prairie dog (Cynomys ludovicianus) towns remaining in
North America. The black-tailed prairie dog is considered
a keystone species that can modify assemblages of small
mammals (Ceballos et al., 1999; Cully et al., 2010);
therefore, this species may influence rodent-borne
zoonotic disease dynamics, which makes this study area
an interesting place to investigate pathogens associated
with wild rodents. Additionally, we chose this area because
there are human settlements and farming activities within
it that could increase human–wildlife contacts.
Fieldwork was conducted on JCGC, which is located
within the grasslands and scrublands of northwestern
Chihuahua (around 30850 0 N, 108825 0 W) approximately
50 km south of the Mexico–United States border
(Ceballos et al., 1999). The study area is part of the
Biosphere Reserve of Janos, a priority area for conservation in Mexico (List et al., 2010). The study consisted of
two sampling sites in each of the following habitat types
(totaling six sampling sites): (1) grasslands without
prairie dogs colonies, (2) grasslands with active prairie
dogs colonies, and (3) mesquite (Prosopis) scrublands.
The grasslands consisted of grasses and annual herbs such
as Bouteloa, Aristida hamulosa, and Fouqueria splendens. In
each sampling site we established a 7 · 7 grid consisting
of 49 Sherman traps (8 · 8 · 23 cm; H. B. Sherman traps,
Tallahassee, FL) with traps set at 10-m intervals (3,600 m2)
and baited with a mixture of rolled oats, peanut butter,
and vanilla extract. Each grid was considered independent and separated by at least 300 m (Ceballos et al.,
1999). We sampled each sampling site during three
consecutive nights over two sampling periods (December
2007 and April 2008). Once captured, we identified,
591
weighed, sexed, and ear-tagged the animals. We collected
blood from the retro-orbital sinus (~0.1 mL) using
capillary tubes and transferred the blood to Nobuto
blood filter strips (Cole-Parmer, Vernon Hills, IL). After
handling, we released animals at their sites of capture.
Procedures for trapping and handling rodents met the
guidelines approved by the American Society of Mammalogists (Sikes et al., 2011) and were approved by the
animal care committee of the Universidad Nacional
Autónoma de México and by the Secretarı́a de Medio
Ambiente y Recursos Naturales, Mexico (license no.
FAUT-0250).
At each habitat type we recorded the number of
individuals captured, species richness (S), and the Shannon diversity index (H; Krebs, 1989). We performed the
serological tests at the Department of Pathology, University
of Texas Medical Branch at Galveston. Serum samples were
tested for immunoglobulin G reactive against Caño
Delgadito virus strain VHV-574, using an enzyme-linked
immunosorbent assay described previously (Fulhorst et al.,
1997). Caño Delgadito virus is highly cross-reactive with
North American hantaviruses such as Sin Nombre virus
and Black Creek Canal virus (Fulhorst et al., 1997). This
strain has been used in other serological surveys of
hantavirus in North America (e.g., Mantooth et al., 2001;
Milazzo et al., 2012). Moreover, Caño Delgadito antibodypositive rodents have reported El Moro Canyon virus,
Limestone Canyon virus, or Sin Nombre virus infections
(by deoxyribonucleic acid sequencing, not virus isolation;
Milazzo et al., 2012). We used a lysate of Vero E6 cells
infected with strain VHV-574 as test antigen. The control
antigen was a lysate of uninfected Vero E6 cells. Serial
fourfold dilutions (from 1:80 through 1:5,120) of each
blood sample were tested against the test antigen and the
control antigen. We used a mixture of immunoglobulin G
anti-Rattus norvegicus peroxidase conjugate and anti-Peromyscus leucopus peroxidase conjugate in conjunction with
the 2,2 0 -Azino-di-(3-ethylbenzthiazoline-6-sulfonate (ABTS)
microwell peroxidase substrate system (Kirkegaard and
Perry Laboratories, Gaithersburg, MD) to detect linked
immunoglobulins. Optical densities (OD) at 405 nm
(reference = 490 nm) were measured with a Dynex MRX
II microplate reader (Dynatech Industries, Inc., McLean,
VA). The adjusted OD (AOD) of a blood–antigen reaction
was the OD of the well coated with the test antigen minus
the OD of the well coated with the control antigen. We
considered a serum sample as positive if the AOD at 1:80
was ‡0.200, the AOD at 1:320 was ‡0.200, and the sum of
the AODs for the series of fourfold dilutions (from 1:80
through 1:5,120) was ‡0.750. The titer of a positive sample
was the reciprocal of the highest dilution for which the
AOD was ‡0.200.
We captured a total of 149 rodents during 1,764 trapnights, representing 11 species, eight genera, and two
families (Heteromyidae and Cricetidae; Table 1). There
was a marked difference in trapping success (number of
592
vol. 59, no. 4
The Southwestern Naturalist
TABLE 1—Rodents tested for hantavirus antibodies in grassland with prairie dog colonies (GLPD), grassland without prairie dog
colonies (GL), and mesquite scrublands (MS) in the Janos–Nuevo Casas Grandes prairie dog complex, in Chihuahua, Mexico.
Number of positive individuals is in parentheses.
Habitat type
GLPD
GL
MS
Rodent species
December
April
December
April
December
April
Baiomys taylori
Dipodomys merriami
Dipodomys ordii
Dipodomys spectabilis
Neotoma albigula
Onychomys leucogaster
Peromyscus leucopus
Peromyscus maniculatus
Perognathus flavus
Reithrodontomys megalotis
Sigmodon hispidus
Overall prevalence (%)
—
—
—
—
—
9
—
—
4
—
—
0
—
1
—
—
—
—
—
—
1
—
—
0
25
2
—
3
2
6
—
9 (3)
5
—
—
5.77
1
—
—
2
—
—
—
—
—
—
—
0
—
18
1
1
7
7
1
13
3
0
5
0
—
8
2
1
—
—
—
4
3
1
4
0
individuals captured/trapping effort) between sampling
periods (0.14 individuals/trap-night in December 2007
and 0.03 individuals/trap-night in April 2008; Table 1).
Four rodent species captured in the study area have been
previously identified as potential hantavirus reservoir
species: Peromyscus maniculatus, P. leucopus, Reithrodontomys
megalotis, and Sigmodon hispidus (Hjelle and Torres-Pérez,
2010). Of these, P. maniculatus was the most abundant
species, with 26 individuals captured (17.45%; Table 1).
Rodents were mainly captured in the mesquite scrublands
(53%, S = 10, H = 1.9), followed by grasslands (37%, S =
7; H = 1.57) and prairie dog grasslands (10%, S = 3; H =
0.85). None of the potential hantavirus-reservoir hosts was
captured in prairie dog grasslands (Table 1). Three P.
maniculatus (~11%), all captured in grasslands and in the
first sampling period, were antibody positive (Table 1).
No other species tested positive. This is the first
documented occurrence of hantavirus antibodies in
rodents from JCGC, as well as from the state of
Chihuahua.
Peromyscus maniculatus is the main reservoir of Sin
Nombre virus, which is the leading cause of HPS in the
United States (Monroe et al., 1999). Sin Nombre virus has
been reported in Mexico, specifically in P. maniculatus (in
the states of Nuevo León, San Luis Potosı́, and Veracruz),
Peromyscus eremicus (in Nuevo León state), P. leucopus (in
Tamaulipas state), and R. megalotis (in Zacatecas state;
Hjelle et al., 1995; Milazzo et al., 2012). Because of high
cross-reactivity of the serological analyses conducted in
this study, it is not possible to determine which hantavirus
is circulating in the study area. To address this, further
molecular analyses are needed.
The black-tailed prairie dog is a keystone species from
the grasslands of North America that can modulate the
assemblages of small mammals within their colonies
(Ceballos et al., 1999; Cully et al., 2010). Additionally,
hantavirus dynamics in rodent hosts may be influenced by
abundance, diversity, and composition structure of small
mammal assemblages (Clay et al., 2009; Suzán et al, 2009;
Carver et al., 2011). Our findings showed that only P.
maniculatus inhabiting grasslands without prairie dogs
were antibody positive. Although our sample size is too
small to claim that habitat type influences hantavirus
prevalence, the fact that P. maniculatus and other
potential hantavirus reservoir hosts are absent or rare in
grasslands with prairie dog colonies in the JCGC
(Cruzado, 2008; Rubio, unpub. data) suggests that prairie
dog colonies may buffer hantavirus transmission. However, to address this topic, as well as temporal dynamics of
hantavirus and rodent populations and communities, a
more extensive study should be conducted. Recognition
of hantavirus distribution and reservoir host ecology in
Mexico will enhance prevention and control of emerging
hantavirus diseases.
We thank S. Ortiz, C. Muñoz, and E. Rendón (Facultad de
Medicina Veterinaria y Zootecnia, Universidad Nacional
Autónoma de México [FMVZ, UNAM]) for field assistance
and O. Rico (FMVZ, UNAM) for detailed comments. We are
grateful to M. L. Milazzo and J. Estrada (University of Texas
Medical Branch), who helped with the serological analyses. Lab
analyses were financially supported by Natonal Institutes of
Health grant AI-41435. This research was supported by
Coordinación de Estudios de Posgrado and Instituto de
Ecologı́a, UNAM. G. S. acknowledges the support provided by
Dirección General de Asuntos del Personal Académico, UNAM
(DGAPA-UNAM) and Consejo Nacional de Ciencia y
Teconologı́a (CONACyT).
LITERATURE CITED
CARVER, S., J. T. TRUEAX, R. DOUGLASS, AND A. KUENZI. 2011.
Delayed density-dependent prevalence of Sin Nombre virus
December 2014
Note
infection in deer mice (Peromyscus maniculatus) in central and
western Montana. Journal of Wildlife Diseases 47:56–63.
CASTRO-ARELLANO, I., G. SUZÁN, R. F. LEÓN, R. M. JIMÉNEZ, AND T. E.
LACHER. 2009. Survey for antibody to hantaviruses in
Tamaulipas, Mexico. Journal of Wildlife Diseases 45:207–212.
CEBALLOS, G., E. MELLINK, AND L. R. HANEBURY. 1993. Distribution
and conservation status of prairie dogs (Cynomys mexicanus)
and (Cynomys ludovicianus) in Mexico. Biological Conservation 63:105–112.
CEBALLOS, G., J. PACHECO, AND R. LIST. 1999. Influence of prairie
dogs (Cynomys ludovicianus) on habitat heterogeneity and
mammalian diversity in Mexico. Journal of Arid Environments 41:161–172.
CHILDS, J. E., T. G. KSIAZEK, C. F. SPIROPOULOU, J. W. KREBS, S.
MORZUNOV, G. O. MAUPIN, K. L. GAGE, P. E. ROLLIN, J. SARISKY, R.
E. ENSCORE, J. K. FREY, C. J. PETERS, AND S. T. NICHOL. 1994.
Serologic and genetic identification of Peromyscus maniculatus
as the primary rodent reservoir for a new hantavirus in the
southwestern United States. Journal of Infectious Diseases
169:1271–1280.
CHU, Y. K., R. D. OWEN, C. SÁNCHEZ-HERNÁNDEZ, M. D. L. ROMEROALMARAZ, AND C. B. JONSSON. 2008. Genetic characterization
and phylogeny of a hantavirus from Western Mexico. Virus
Research 131:180–188.
CLAY, C. A., E. M. LEHMER, S. S. JEOR, AND M. D. DEARING. 2009. Sin
Nombre virus and rodent species diversity: a test of the
dilution and amplification hypotheses. PlosOne 4:10.1371/
journal.pone.0006467 e6467.
CRUZADO, J. 2008. Dinámica poblacional y estructura de la
comunidad de pequeños mamı́feros de la región Janos-Casas
Grandes, Chihuahua. M.S. thesis, Universidad Nacional
Autónoma de México, México, D.F., México.
CULLY, J. F., S. K. COLLINGE, R. E. VANNIMWEGEN, C. RAY, W. C.
JOHNSON, B. THIAGARAJAN, D. B. CONLIN, AND B. E. HOLMES. 2010.
Spatial variation in keystone effects: small mammal diversity
associated with black-tailed prairie dog colonies. Ecography
33:667–677.
FULHORST, C. F., M. C. MONROE, R. A. SALAS, G. DUNO, A. UTRERA, T.
G. KSIAZEK, S. T. NICHOL, N. M DE MANZIONE, D. TOVAR, AND R.
B. TESH. 1997. Isolation, characterization and geographic
distribution of Cano Delgadito virus, a newly discovered
South American hantavirus (family Bunyaviridae). Virus
Research 51:159–171.
HJELLE, B., AND F. TORRES-PÉREZ. 2010. Hantaviruses in the
Americas and their role as emerging pathogens. Viruses
2:2559–2586.
HJELLE, B., B. ANDERSON, N. TORREZ-MARTÍNEZ, W. SONG, W. L.
GANNON, AND T. L. YATES. 1995. Prevalence and geographic
genetic variation of hantaviruses of New World harvest mice
(Reithrodontomys): identification of a divergent genotype from
a Costa Rican Reithrodontomys mexicanus. Virology 207:452–
459.
HJELLE, B., N. TORREZ-MARTÍNEZ, AND F. KOSTER. 1996. Hantavirus
pulmonary syndrome-related virus from Bolivia. Lancet
347:57.
JONSSON, C. B., L. T. MORAES FIGUEIREDO, AND O. VAPALAHTI. 2010. A
global perspective on hantavirus ecology, epidemiology, and
disease. Clinical Microbiology Reviews 23:412–441.
KARIWA, H., H. YOSHIDA, C. SANCHEZ-HERNANDEZ, M. DE L. ROMEROALMARAZ, J. A ALMAZAN-CATALAN, C. RAMOS, D. MIYASHITA, T.
SETO, A. TAKANO, M. TOTANI, R. MURATAA, N. SAASAA, M.
ISHIZUKAA, T. SANADAA, K. YOSHIIA, K. YOSHIMATSUD, J. ARIKAWAA,
593
AND I. TAKASHIMAA. 2012. Genetic diversity of hantaviruses in
Mexico: identification of three novel hantaviruses from
Neotominae rodents. Virus Research 163:486–494.
KLEIN, S. L, M. C. ZINK, AND G. E. GLASS. 2004. Seoul virus
increases aggressive behaviour in male Norway rats. Animal
Behaviour 67:421–429.
KREBS, C. J. 1989. Ecological methodology. Harper Collins, New
York.
LIST, R., J. PACHECO, E. PONCE, R. SIERRA-CORONA, AND G. CEBALLOS.
2010. The Janos Biosphere Reserve, Northern Mexico.
International Journal of Wilderness 16:35–41.
MANTOOTH, S. J., M. L. MILAZZO, R. D. BRADLEY, C. L. HICE, G.
CEBALLOS, R. B. TESH, AND C. F. FULHORST. 2001. Geographical
distribution of rodent-associated hantaviruses in Texas.
Journal of Vector Ecology 26:7–14.
MILAZZO, M. L., M. N. CAJIMAT, H. E. ROMO, J. G. ESTRADA-FRANCO,
L. I. IÑIGUEZ-DÁVALOS, R. D. BRADLEY, AND C. F. FULHORST. 2012.
Geographic distribution of hantaviruses associated with
Neotomine and Sigmodontine rodents, Mexico. Emerging
Infectious Diseases 18:571–576.
MILLS, J. N., J. M. JOHNSON, T. G. KSIAZEK, B. A. ELLIS, P. E. ROLLIN,
T. L. YATES, M. O. MANN, M. R. JOHNSON, M. L. CAMPBELL, AND J.
MIYASHIRO. 1998. A survey of hantavirus antibody in smallmammal populations in selected United States National
Parks. American Journal of Tropical Medicine and Hygiene
58:525–532.
MILLS, J. N., T. G. KSIAZEK, B. A. ELLIS, P. E. ROLLIN, S. T. NICHOL, T.
L. YATES, W. L. GANNON, C. E. LEVY, D. M. ENGELTHALER, T. DAVIS,
D. T. TANDA, J. W. FRAMPTON, C. R. NICHOLS, C. J. PETERS, AND J.
E. CHILDS. 1997. Patterns of association with host and habitat:
antibody reactive with Sin Nombre virus in small mammals in
the major biotic communities of the southwestern United
States. American Journal of Tropical Medicine and Hygiene
56:273–284.
MILLS, J. N., T. G. KSIAZEK, C. PETERS, AND J. E. CHILDS. 1999. Longterm studies of hantavirus reservoir populations in the
southwestern United States: a synthesis. Emerging Infectious
Diseases 5:135–142.
MONROE, M. C., S. P. MORZUNOV, A. M. JOHNSON, M. D. BOWEN, H.
ARTSOB, T. YATES, C. PETERS, P. E. ROLLIN, T. G. KSIAZEK, AND S. T.
NICHOL. 1999. Genetic diversity and distribution of Peromyscusborne hantaviruses in North America. Emerging Infectious
Diseases 5:75–86.
SIKES, R. S., W. L. GANNON, AND THE ANIMAL CARE AND USE
COMMITTEE. 2011. Guidelines of the American Society of
Mammalogists for the use of wild mammals in research.
Journal of Mammalogy 92:235–253.
SUZÁN, G., G. CEBALLOS, J. MILLS, T. G. KSIAZEK, AND T. YATES. 2001.
Serologic evidence of hantavirus infection in sigmodontine
rodents in Mexico. Journal of Wildlife Diseases 37:391–393.
SUZÁN, G., E. MARCE, J. T. GIERMAKOWSKI, J. N. MILLS, G. CEBALLOS,
R. S. OSTFELD, B. ARMIEN, J. M. PASCALE, AND, T. L. YATES. 2009.
Experimental evidence for reduced rodent diversity causing
increased hantavirus prevalence. PlosOne 4:PMC2673579.
TORO, J., J. D. VEGA, A. S. KHAN, J. N. MILLS, P. PADULA, W. TERRY, Z.
YADÓN, R. VALDERRAMA, B. A. ELLIS, AND C. PAVLETIC. 1998. An
outbreak of hantavirus pulmonary syndrome, Chile, 1997.
Emerging Infectious Diseases 4:687–694.
VÁZQUEZ-PÉREZ, J., Y. MORENO-VALENCIA, AND R. PÉREZ-PADILLA. 2012.
¿Dónde están las neumonı́as por hantavirus en México?.
Neumologı́a y Cirugı́a de Tórax 71:287–288.
VINCENT, M. J., E. QUIROZ, F. GRACIA, A. J. SANCHEZ, T. G. KSIAZEK, P.
594
The Southwestern Naturalist
T. KITSUTANI, L. A. RUEDAS, D. S. TINNIN, L. CACERES, AND A.
GARCIA. 2000. Hantavirus pulmonary syndrome in Panama:
identification of novel hantaviruses and their likely reservoirs. Virology 277:14–19.
YATES, T. L., J. N. MILLS, C. A. PARMENTER, T. G . KSIAZEK, R. R.
PARMENTER, J. R. VANDE CASTLE, C. H. CALISHER, S. T. NICHOL,
K. D. ABBOTT, J. C. YOUNG, M. L. M. L. MORRISON, B. J. BEATY, J.
L. DUNNUM, R. J. BAKER, J. SALAZAR-BRAVO, AND C. J. PETERS.
vol. 59, no. 4
2002. The ecology and evolutionary history of an emergent
disease: hantavirus pulmonary syndrome. Bioscience
52:989–998.
Submitted 8 April 2014.
Acceptance recommended by Associate Editor, Stephen G. Mech, 15
August 2014.